Odour Processing By Principal Neurons of the Piriform Cortex In Vivo

Description

The piriform cortex (PC) is important for the cortical processing
of olfactory information. The PC is widely viewed as a pattern
recognition device whose primary function is the formation of
‘odour objects’, that is, the perception of complex odours
comprising many chemical components as single olfactory percepts
(e.g. the scent of a rose), a task that is heavily dependent on
the intracortical associational network. Two types of
glutamatergic principal neurons...[Show more] are present in approximately
equal numbers in layer 2 of the PC: semilunar (SL) and
superficial pyramidal (SP) cells. Despite a long-standing
misconception that the principal neurons of the PC are a
functionally homogenous population, recent work has shown that SL
and SP cells differ significantly in their connectivity and in
vitro electrophysiology. Specifically, emerging data has
indicated that intracortical connectivity increases with
increasingly deep somatic locations, suggesting that, in response
to olfactory stimulation, cortical computations shift from
afferent (sensory) processing to associative processing down the
PC superficial-to-deep axis. In light of the important
differences between the two main classes of principal neurons, we
hypothesised that SL and SP cells contribute differentially to
the cortical processing of olfactory sensory information.
In this thesis, we examined the odour responses of layer 2
principal neurons in the anterior PC using whole-cell patch clamp
electrophysiology. We show that odour responses are highly
variable and richly nuanced in vivo; however, they can be broadly
separated into three basic categories: excitation, inhibition and
unresponsiveness. Our current clamp data revealed that an
intrinsic property, the spike after-hyperpolarisation (AHP),
correlates strongly with the somatic laminar depth, suggesting
that the AHP could be used to identify neurons (SL or SP cells)
recorded in vivo. Importantly, current clamp data indicate that
olfactory excitatory tuning correlates strongly with the AHP in
vivo, such that putative SP cells (characterised by a small AHP)
are more broadly excited by odours than putative SL cells
(characterised by a large AHP), presumably due to a difference in
intracortical connectivity. These results further suggest that,
rather than assuming a sharp dichotomy of neuronal phenotypes,
SL-like cells gradually transition into SP-like cells along the
cortical superficial-to-deep axis.
Voltage clamp data indicate that principal neurons are under a
substantial level of tonic inhibition in the absence of odour. We
show that spontaneous and odour-evoked inhibition dominates and
scales with excitation under physiological conditions. These
results suggest that local inhibition contributes to the reported
sparse odour coding in the cortex.
Overall, these data are consistent with our proposed model of the
anterior PC excitatory network, which posits that 1) principal
neuron phenotype transitions smoothly across the cortical
superficial-to-deep axis and 2) principal neurons become
increasingly incorporated into the local intracortical
microcircuits with increasingly deep somatic location, as a
result, 3) neuronal excitatory tuning becomes progressively
broader with increasing somatic depth. These results suggest that
SL cells may be important for decorrelating overlapping input
patterns and hence preserving the salient olfactory attributes of
an odour, whereas SP cells are more heavily implicated in the
associative aspect of olfactory processing.